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打哈欠行为进化中的惯性与快速分化:两种亲缘关系相近但社会行为不同的猴子之间的比较

Inertia and Rapid Divergence in the Evolution of Yawning: A Comparison Between Two Closely Related but Socially Different Monkeys.

作者信息

Pedruzzi Luca, Maglieri Veronica, Oliveri Paolo, Francesconi Martina, Riccobono Rea, Bigozzi Filippo, Lemasson Alban, Palagi Elisabetta

机构信息

EthoS (Ethologie Animale et Humaine), U.M.R 6552, Université de Rennes, Université de Normandie, CNRS, Rennes, France.

Unit of Ethology, Department of Biology, University of Pisa, Pisa, Italy.

出版信息

Am J Primatol. 2025 Jun;87(6):e70049. doi: 10.1002/ajp.70049.

DOI:10.1002/ajp.70049
PMID:40437861
Abstract

Complex communication systems appear to evolve alongside social complexity. Comparing closely related species with similar social structures but distinct sociobiology offers valuable insights into the evolution of communicative variability. Here, we explore yawning (morphology, sensory modalities, contexts, contagious effect), a highly conserved behavioral trait, in two zoo-housed groups of geladas (Theropithecus gelada, n = 67, n = 1422) and hamadryas baboons (Papio hamadryas, n = 28, n = 602). The species are optimal candidates as they both form multilevel groups but differ in intra-group dynamics, cohesion, and cross-sex bonding. Although both species displayed distinct yawn morphologies, hamadryas yawned less frequently than geladas, mainly in non-social contexts and without vocalization. In contrast, geladas yawned more often during affiliative interactions, highlighting a more social dimension to their yawns. When focusing on silent yawns, hamadryas showed a male-biased yawning frequency, whereas geladas exhibited similar rates between sexes, suggesting a more prominent female role in their yawning patterns. We found that yawning is contagious not only in geladas, as previously known, but also in hamadryas baboons. However, geladas were more responsive to others' yawns, possibly due to their greater communicative complexity or to the need to maintain cohesion in larger groups. In geladas, both sexes exhibited similar levels of yawn contagion, whereas in hamadryas it was predominantly male-driven, reflecting the central role of males in hamadryas social dynamics. Our study suggests both evolutionary inertia and divergence in Papionine yawning evolution. The findings confirm the derived nature of gelada yawn vocalizations and highlight the link between multimodal communication and social complexity. Moreover, geladas exhibit more nuanced, context-dependent yawning, likely shaped by their intricate sociobiology. In contrast, hamadryas display a more male-dominated yawning pattern, reflecting their distinct social dynamics. To fully understand the ecological significance of this ancient behavior, further cross-species research on yawning and its contagious effect in wild populations is essential.

摘要

复杂的通讯系统似乎是随着社会复杂性一同进化的。比较具有相似社会结构但社会生物学特征不同的近缘物种,能为探究通讯变异性的进化提供宝贵见解。在此,我们对圈养在动物园的两组狒狒(狮尾狒,Theropithecus gelada,n = 67,n = 1422)和阿拉伯狒狒(Papio hamadryas,n = 28,n = 602)的打哈欠行为(形态、感觉方式、情境、传染性效应)进行了探究,打哈欠是一种高度保守的行为特征。这两个物种是理想的研究对象,因为它们都形成多层次群体,但在群体内部动态、凝聚力和跨性别联系方面存在差异。尽管两个物种都表现出独特的哈欠形态,但阿拉伯狒狒打哈欠的频率低于狮尾狒,主要在非社交情境下且不发声。相比之下,狮尾狒在亲和互动期间打哈欠更频繁,这凸显了它们打哈欠行为更具社交性的一面。当聚焦于无声哈欠时,阿拉伯狒狒的哈欠频率呈现出雄性偏向,而狮尾狒两性的哈欠频率相似,这表明在它们的哈欠模式中雌性的作用更为突出。我们发现,打哈欠不仅如之前所知在狮尾狒中具有传染性,在阿拉伯狒狒中同样具有传染性。然而,狮尾狒对其他个体的哈欠反应更强烈,这可能是由于它们具有更高的通讯复杂性,或者是由于在更大群体中维持凝聚力的需要。在狮尾狒中,两性表现出相似程度的哈欠传染性,而在阿拉伯狒狒中,哈欠传染性主要由雄性驱动,这反映了雄性在阿拉伯狒狒社会动态中的核心作用。我们的研究表明,狒狒打哈欠行为的进化既存在惯性又有分歧。这些发现证实了狮尾狒哈欠发声的衍生性质,并突出了多模态通讯与社会复杂性之间 的联系。此外,狮尾狒表现出更细微、依赖情境的打哈欠行为,这可能是由其复杂的社会生物学所塑造的。相比之下,阿拉伯狒狒表现出更以雄性为主导的哈欠模式,这反映了它们独特的社会动态。为了全面理解这种古老行为的生态意义,对野生种群中打哈欠及其传染性效应进行进一步的跨物种研究至关重要。

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Inertia and Rapid Divergence in the Evolution of Yawning: A Comparison Between Two Closely Related but Socially Different Monkeys.打哈欠行为进化中的惯性与快速分化:两种亲缘关系相近但社会行为不同的猴子之间的比较
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本文引用的文献

1
Yawning in sync: implications for social cohesion in horses.同步打哈欠:对马群社会凝聚力的影响
Curr Zool. 2024 Sep 16;71(2):137-151. doi: 10.1093/cz/zoae052. eCollection 2025 Apr.
2
Yawn Contagion and Modality-Matching in the Female-Bonded Society of Geladas (Theropithecus gelada).狮尾狒(狮尾狒属)雌性群居社会中的打哈欠传染与模态匹配
Am J Primatol. 2025 Jan;87(1):e23709. doi: 10.1002/ajp.23709.
3
First predict, then bond: Rethinking the function of mimicry from prediction to affiliation in human and non-human animals.
先预测,再联结:重新思考人类和非人类动物中从预测到归属的拟态功能。
Neurosci Biobehav Rev. 2025 Jan;168:105950. doi: 10.1016/j.neubiorev.2024.105950. Epub 2024 Nov 21.
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More than a simple fixed action pattern: Yawning in drills.不只是简单的固定行为模式:打哈欠在操练中。
Primates. 2024 Jul;65(4):281-297. doi: 10.1007/s10329-024-01127-7. Epub 2024 Apr 22.
5
The sound of yawns makes geladas yawn.打哈欠的声音会使鬼脸金丝猴也跟着打哈欠。
Sci Rep. 2024 Jan 7;14(1):361. doi: 10.1038/s41598-023-49797-5.
6
Social Cognitive Correlates of Contagious Yawning and Smiling.传染性打哈欠和微笑的社会认知相关性。
Hum Nat. 2023 Dec;34(4):569-587. doi: 10.1007/s12110-023-09463-1. Epub 2023 Nov 15.
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Yawning and scratching contagion in wild spider monkeys (Ateles geoffroyi).野生蜘蛛猴(Ateles geoffroyi)中的打哈欠和抓挠的传染性。
Sci Rep. 2023 May 24;13(1):8367. doi: 10.1038/s41598-023-35693-5.
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Contagious yawning in African painted dogs.非洲斑鬣狗的传染性打哈欠。
Anim Cogn. 2023 Jul;26(4):1191-1198. doi: 10.1007/s10071-023-01766-1. Epub 2023 Mar 16.
9
Inter-sexual multimodal communication during mating in wild geladas: the leading role of females.野生狮尾狒交配过程中的两性多模态交流:雌性的主导作用
Curr Zool. 2021 Nov 9;68(5):570-580. doi: 10.1093/cz/zoab093. eCollection 2022 Oct.
10
Familiarity modulates both intra- and interspecific yawn contagion in red-capped mangabeys.熟悉度调节红帽卷尾猴的个体内和种间哈欠传染。
Sci Rep. 2022 Jul 1;12(1):11138. doi: 10.1038/s41598-022-15395-0.